Natural selection and repeated patterns of molecular evolution following allopatric divergence

  1. Yibo Dong
  2. Shichao Chen
  3. Shifeng Cheng
  4. Wenbin Zhou
  5. Qing Ma
  6. Zhiduan Chen
  7. Cheng-Xin Fu
  8. Xin Liu  Is a corresponding author
  9. Yun-peng Zhao  Is a corresponding author
  10. Pamela S Soltis  Is a corresponding author
  11. Gane Ka-Shu Wong  Is a corresponding author
  12. Douglas E Soltis  Is a corresponding author
  13. Jenny Xiang  Is a corresponding author
  1. North Carolina State University, United States
  2. University of Florida, United States
  3. Beijing Genomics Institute, China
  4. Chinese Academy of Sciences, China
  5. Zhejiang University, China

Abstract

Although geographic isolation is a leading driver of speciation, the tempo and pattern of divergence at the genomic level remain unclear. We examine genome-wide divergence of putatively single-copy orthologous genes (POGs) in 20 allopatric species/variety pairs from diverse angiosperm clades, with 16 pairs reflecting the classic eastern Asia-eastern North America floristic disjunction. In each pair, >90% of POGs are under purifying selection, and <10% are under positive selection. A set of POGs are under strong positive selection, 14 of which are shared by 10-15 pairs, and one shared by all pairs; 15 POGs are annotated to biological processes responding to various stimuli. The relative abundance of POGs under different selective forces exhibits a repeated pattern among pairs despite an ~10-million-year difference in divergence time. Species divergence times are positively correlated with abundance of POGs under moderate purifying selection, but negatively correlated with abundance of POGs under strong purifying selection.

Data availability

Sequences of ortologous gene families and pairs of POGs sequences used for calculation of Ka and Ks have been submitted to Dryad (https://datadryad.org//). Raw transcriptome data have been submitted to NCBI SRA database with Bioproject number PRJNA508825 and Biosample number from SAMN10534244 to SAMN10534283 (Supplementary File 11).

The following data sets were generated

Article and author information

Author details

  1. Yibo Dong

    Department of Plant and Microbial Biology, North Carolina State University, Raleigh, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Shichao Chen

    Florida Museum of Natural History, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Shifeng Cheng

    Beijing Genomics Institute, Shenzhen, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Wenbin Zhou

    Department of Plant and Microbial Biology, North Carolina State University, Raleigh, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Qing Ma

    Department of Plant and Microbial Biology, North Carolina State University, Raleigh, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Zhiduan Chen

    State Key Laboratory of Systematic and Evolutionary Botany, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Cheng-Xin Fu

    Laboratory of Systematic & Evolutionary Botany and Biodiversity, Zhejiang University, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Xin Liu

    Beijing Genomics Institute, Shenzen, China
    For correspondence
    liuxin@genomics.cn
    Competing interests
    The authors declare that no competing interests exist.
  9. Yun-peng Zhao

    Laboratory of Systematic & Evolutionary Botany and Biodiversity, Zhejiang University, Hangzhou, China
    For correspondence
    ypzhao913@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  10. Pamela S Soltis

    Florida Museum of Natural History, University of Florida, Gainesville, United States
    For correspondence
    psoltis@flmnh.ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
  11. Gane Ka-Shu Wong

    Beijing Genomics Institute, Shenzen, China
    For correspondence
    gane@ualberta.ca
    Competing interests
    The authors declare that no competing interests exist.
  12. Douglas E Soltis

    Florida Museum of Natural History, University of Florida, Gainesville, United States
    For correspondence
    dsoltis@ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
  13. Jenny Xiang

    Department of Plant and Microbial Biology, North Carolina State University, Raleigh, United States
    For correspondence
    jenny_xiang@ncsu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9016-0678

Funding

National Science Foundation (DEB-442161)

  • Yibo Dong
  • Wenbin Zhou
  • Jenny Xiang

National Science Foundation (DEB-442280)

  • Shichao Chen
  • Pamela S Soltis
  • Douglas E Soltis

National Science Foundation of China (IOS-024629)

  • Shichao Chen
  • Yun-peng Zhao

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2019, Dong et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,371
    views
  • 536
    downloads
  • 21
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Yibo Dong
  2. Shichao Chen
  3. Shifeng Cheng
  4. Wenbin Zhou
  5. Qing Ma
  6. Zhiduan Chen
  7. Cheng-Xin Fu
  8. Xin Liu
  9. Yun-peng Zhao
  10. Pamela S Soltis
  11. Gane Ka-Shu Wong
  12. Douglas E Soltis
  13. Jenny Xiang
(2019)
Natural selection and repeated patterns of molecular evolution following allopatric divergence
eLife 8:e45199.
https://doi.org/10.7554/eLife.45199

Share this article

https://doi.org/10.7554/eLife.45199

Further reading

    1. Developmental Biology
    2. Evolutionary Biology
    Simon Rethemeier, Sonja Fritzsche ... Vera S Hunnekuhl
    Research Article

    The insect brain and the timing of its development underwent evolutionary adaptations. However, little is known about the underlying developmental processes. The central complex of the brain is an excellent model to understand neural development and divergence. It is produced in large parts by type II neuroblasts, which produce intermediate progenitors, another type of cycling precursor, to increase their neural progeny. Type II neuroblasts lineages are believed to be conserved among insects, but little is known on their molecular characteristics in insects other than flies. Tribolium castaneum has emerged as a model for brain development and evolution. However, type II neuroblasts have so far not been studied in this beetle. We created a fluorescent enhancer trap marking expression of Tc-fez/earmuff, a key marker for intermediate progenitors. Using combinatorial labeling of further markers, including Tc-pointed, we characterized embryonic type II neuroblast lineages. Intriguingly, we found nine lineages per hemisphere in the Tribolium embryo while Drosophila produces only eight per brain hemisphere. These embryonic lineages are significantly larger in Tribolium than they are in Drosophila and contain more intermediate progenitors. Finally, we mapped these lineages to the domains of head patterning genes. Notably, Tc-otd is absent from all type II neuroblasts and intermediate progenitors, whereas Tc-six3 marks an anterior subset of the type II lineages. Tc-six4 specifically marks the territory where anterior-medial type II neuroblasts differentiate. In conclusion, we identified a conserved pattern of gene expression in holometabolan central complex forming type II neuroblast lineages, and conserved head patterning genes emerged as new candidates for conferring spatial identity to individual lineages. The higher number and greater lineage size of the embryonic type II neuroblasts in the beetle correlate with a previously described embryonic phase of central complex formation. These findings stipulate further research on the link between stem cell activity and temporal and structural differences in central complex development.

    1. Evolutionary Biology
    William R Thomas, Troy Richter ... Liliana M Davalos
    Research Article

    Contrasting almost all other mammalian wintering strategies, Eurasian common shrews, Sorex araneus, endure winter by shrinking their brain, skull, and most organs, only to then regrow to breeding size the following spring. How such tiny mammals achieve this unique brain size plasticity while maintaining activity through the winter remains unknown. To discover potential adaptations underlying this trait, we analyzed seasonal differential gene expression in the shrew hypothalamus, a brain region that both regulates metabolic homeostasis and drastically changes size, and compared hypothalamus gene expression across species. We discovered seasonal variation in suites of genes involved in energy homeostasis and apoptosis, shrew-specific upregulation of genes involved in the development of the hypothalamic blood-brain barrier and calcium signaling, as well as overlapping seasonal and comparative gene expression divergence in genes implicated in the development and progression of human neurological and metabolic disorders, including CCDC22. With high metabolic rates and facing harsh winter conditions, S. araneus have evolved both adaptive and plastic mechanisms to sense and regulate their energy budget. Many of these changes mirrored those identified in human neurological and metabolic disease, highlighting the interactions between metabolic homeostasis, brain size plasticity, and longevity.